Expression of MAP1B protein and its phosphorylated form MAP1B-P in the CNS of a continuously growing fish, the rainbow trout

Brain Research

Volumn 1009, Issue 1-2, 2004, Pages 54-66

  Alfei, Laura ^a   Soares, Sylvia ^b   Alunni, Alessandro ^a   Ravaille Veron, Michèle ^b   Von Boxberg, Ysander ^b   Nothias, Fatiha ^b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b SORBONNE UNIVERSITÉ   (France)

Author keywords

Anterior octaval nucleus; Aon; Ap; Area postrema; Bs; Cc; Central canal; Central nervous system; Cerebro spinal projection; Cf; Climbing fibers; CNS; Cocb; Corpus cerebelli; Mauthner axon; Microtubule associated protein 1B; Motoneuron; Regeneration; Vulbospinal tract

Indexed keywords

ANTIBODY; FISH PROTEIN; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 5; PROTEIN ANTIBODY;

ANIMAL TISSUE; ARTICLE; CELL SUBPOPULATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CROSS REACTION; DEVELOPMENTAL STAGE; GLIA CELL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MAUTHNER CELL; MOLECULAR WEIGHT; MOTONEURON; NERVE FIBER; NERVE FIBER REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; RAINBOW TROUT; RETINOTECTAL PROJECTION; RHOMBENCEPHALON; RNA PROBE; SENSORY NERVE CELL; SPINAL CORD; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICROTUBULE-ASSOCIATED PROTEINS; ONCORHYNCHUS MYKISS; PHOSPHORYLATION;

EID: 2142694338     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2004.02.043     Document Type: Article

References (77)

1. Aguayo A.J., Rasminsky M., Bray G.M., Carbonetto S., McKerracher L., Villegas-Perez M.P., Vidal-Sanz M., Carter D.A. Degenerative and regenerative responses of injured neurons in the central nervous system of adult mammals. Philos. Trans. R. Soc. Lond., B. Biol. Sci. 331:1991;337-343
2. Alfei L., Medolago Albani L., Mosetti A.R., Scarfo C., Stefanelli A. Cytoskeletal components and calibers in developing fish Mauthner axon (Salmo gairdneri Rich.). J. Comp. Neurol. 314:1991;164-170
3. Alfei L., Medolago-Albani L., Zezze G.M., Stefanelli A. Morphometric analysis of Mauthner axon cytoskeletal components in adult and subadult fish. J. Submicrosc. Cytol. Pathol. 24:1992;115-122
4. Alfei L., Onali A., Caronti B., Valente A.M., Medolago Albani L., Pasqualini C., Denizot J.P. Phosphorylated and non-phosphorylated neurofilament epitopes are co-distributed in the fish Mauthner axon. Cell. Mol. Biol. (Noisy-le-grand). 44:1998;605-614
5. Bastmeyer M., Jeserich G., Stuermer C.A. Similarities and differences between fish oligodendrocytes and Schwann cells in vitro. Glia. 11:1994;300-314
6. Becker T., Wullimann M.F., Becker C.G., Bernhardt R.R., Schachner M. Axonal regrowth after spinal cord transection in adult zebrafish. J. Comp. Neurol. 377:1997;577-595
7. Becker T., Bernhardt R.R., Reinhard E., Wullimann M.F., Tongiorgi E., Schachner M. Readiness of zebrafish brain neurons to regenerate a spinal axon correlates with differential expression of specific cell recognition molecules. J. Neurosci. 18:1998;5789-5803
8. Behrend K., Donicht M. Descending connections from the brainstem to the spinal cord in the electric fish Eigenmannia. Quantitative description based on retrograde horseradish peroxidase and fluorescent-dye transport. Brain Behav. Evol. 35:1990;227-239
9. Benowitz L.I., Leon S., Tabibiazar R., Jin Y., Irwin N. Axonal regeneration in the primary visual pathway of goldfish and rats. Ingoglia N., Murray M. Axonal Regeneration in the Central Nervous System. 2001;45-66 Marcel Dekker, Basal, New York
10. Bernhardt R.R., Tongiorgi E., Anzini P., Schachner M. Increased expression of specific recognition molecules by retinal ganglion cells and by optic pathway glia accompanies the successful regeneration of retinal axons in adult zebrafish. J. Comp. Neurol. 376:1996;253-264
11. Bernstein J.J., Wells M.R., Bernstein M.E. Spinal cord regeneration. CW C. Synaptic Renewal and Neurochemistry, Neuronal Plasticity. 1978;50-71 Raven Press, New York
12. Black M.M., Slaughter T., Fischer I. Microtubule-associated protein 1b (MAP1b) is concentrated in the distal region of growing axons. J. Neurosci. 14:1994;857-870
13. Bosch T.J., Roberts B.L. The size and number of neurons descending to the spinal cord in relation to body length in the European eel (Anguilla anguilla). Brain Behav. Evol. 44:1994;50-60
14. Boyne L.J., Martin K., Hockfield S., Fischer I. Expression and distribution of phosphorylated MAP1B in growing axons of cultured hippocampal neurons. J. Neurosci. Res. 40:1995;439-450
15. Brandstatter R., Kotrschal K. Brain growth patterns in four European cyprinid fish species (Cyprinidae, Teleostei): roach (Rutilus rutilus), bream (Abramis brama), common carp (Cyprinus carpio) and sabre carp (Pelecus cultratus). Brain Behav. Evol. 35:1990;195-211
16. Bunt S.M., Fill-Moebs P. Selection of pathways by regenerating spinal cord fiber tracts. Brain Res. 318:1984;307-311
17. Coggeshall R.E., Birse S.G., Youngblood C.S. Recovery from spinal transection in fish. Neurosci. Lett. 32:1982;259-264
18. Davis B.M., Duffy M.T., Simpson S.B. Jr. Bulbospinal and intraspinal connections in normal and regenerated salamander spinal cord. Exp. Neurol. 103:1989;41-51
19. Davis B.M., Ayers J.L., Koran L., Carlson J., Anderson M.C., Simpson S.B. Jr. Time course of salamander spinal cord regeneration and recovery of swimming: HRP retrograde pathway tracing and kinematic analysis. Exp. Neurol. 108:1990;198-213
20. Edwards M.A., Sharma S.C., Murray M. Selective retinal reinnervation of a surgically created tectal island in goldfish: I. Light microscopic analysis. J. Comp. Neurol. 232:1985;372-385
21. Fischer I., Romano-Clarke G. Changes in microtubule-associated protein MAP1B phosphorylation during rat brain development. J. Neurochem. 55:1990;328-333
22. Fischer I., Konola J., Cochary E. Microtubule associated protein (MAP1B) is present in cultured oligodendrocytes, co-localizes with tubulin. J. Neurosci. Res. 27:1990;112-124
23. Gordon-Weeks P.R., Fischer I. MAP1B expression, microtubule stability in growing, regenerating axons. Microsc. Res. Tech. 48:2000;63-74
24. Hanna G.F., Nawar N.N., Sharma S.C. Regeneration of ascending spinal axons in goldfish. Brain Res. 791:1998;235-245
25. Hirokawa N. Microtubule organization and dynamics dependent on microtubule-associated proteins. Curr. Biol. 6:1994;74-81
26. Jacobson M., Gaze R.M. Selection of appropriate tectal connections by regenerating optic nerve fibers in adult goldfish. Exp. Neurol. 13:1965;418-430
27. Kalman M. Astroglial architecture of the carp (Cyprinus carpio) brain as revealed by immunohistochemical staining against glial fibrillary acidic protein (GFAP). Anat. Embryol. (Berl.). 198:1998;409-433
28. Keirstead H.S., Dyer J.K., Sholomenko G.N., McGraw J., Delaney K.R., Steeves J.D. Axonal regeneration and physiological activity following transection and immunological disruption of myelin within the hatchling chick spinal cord. J. Neurosci. 15:1995;6963-6974
29. Koumans J.T.M., Akster H.A. Myogenic cells in the development and growth of fish. Comp. Biochem. Physiol. 110A:1995;3-20
30. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685
31. Lee R.K., Eaton R.C., Zottoli S.J. Segmental arrangement of reticulospinal neurons in the goldfish hindbrain. J. Comp. Neurol. 329:1993;539-556
32. Leyhausen C., Kirschbaum F., Szabo T., Erdelen M. Differential growth in the brain of the weakly electric fish, Apteronotus leptorhynchus (Gymnotiformes), during ontogenesis. Brain Behav. Evol. 30:1987;230-248
33. Liu D., Fischer I. Structural analysis of the proximal region of the microtubule-associated protein 1B promoter. J. Neurochem. 69:1997;910-919
34. Luiten P.G. Afferent and efferent connections of the optic tectum in the carp (Cyprinus carpio L.). Brain Res. 220:1981;51-65
35. Ma D., Nothias F., Boyne L.J., Fischer I. Differential regulation of microtubule-associated protein 1B (MAP1B) in rat CNS and PNS during development. J. Neurosci. Res. 49:1997;319-332
36. Ma D., Chow S., Obrocka M., Connors T., Fischer I. Induction of microtubule-associated protein 1B expression in Schwann cells during nerve regeneration. Brain Res. 823:1999;141-153
37. Ma D., Connors T., Nothias F., Fischer I. Regulation of the expression and phosphorylation of microtubule-associated protein 1B during regeneration of adult dorsal root ganglion neurons. Neuroscience. 99:2000;157-170
38. Mack T.G., Koester M.P., Pollerberg G.E. The microtubule-associated protein MAP1B is involved in local stabilization of turning growth cones [In Process Citation]. Mol. Cell. Neurosci. 15:2000;51-65
39. Martini R. Expression and functional roles of neural cell surface molecules and extracellular matrix components during development and regeneration of peripheral nerves. J. Neurocytol. 23:1994;1-28
40. Matus A. Microtubule-associated proteins and neuronal morphogenesis. J. Cell Sci., Suppl. 15:1991;61-67
41. Matus A., Riederer B. Microtubule-associated proteins in the developing brain. Ann. N. Y. Acad. Sci. 466:1986;167-179
42. McClellan A.D. Functional regeneration and restoration of locomotor activity following spinal cord transection in the lamprey. Prog. Brain Res. 103:1994;203-217
43. Meek J. Comparative aspects of cerebellar organization. From mormyrids to mammals. Eur. J. Morphol. 30:1992;37-51
44. Meek J., Nieuwenhuys R. Holosteans and Teleost. 1998;Springer, Berlin. 759-937 pp.
45. Modig C., Rutberg M., Detrich H.W. III, Billger M., Stromberg E., Wallin M. MAP 0, a 400-kDa microtubule-associated protein unique to teleost fish. Cell Motil. Cytoskelet. 38:1997;258-269
46. Murray M. Regeneration of retinal axons into the goldfish optic tectum. J. Comp. Neurol. 168:1976;175-195
47. Murray M., Edwards M.A. A quantitative study of the reinnervation of the goldfish optic tectum following optic nerve crush. J. Comp. Neurol. 209:1982;363-373
48. Murray M., Grafstein B. Changes in the morphology and amino acid incorporation of regenerating goldfish optic neurons. Exp. Neurol. 23:1969;544-560
49. Nothias F., Fischer I., Murray M., Mirman S., Vincent J.-D. Expression of a phosphorylated isoform of MAP1B is maintained in adult central nervous system areas that retain capacity for structural plasticity. J. Comp. Neurol. 368:1996;317-334
50. Nothias F., Vernier P., von Boxberg Y., Mirman S., Vincent J.D. Modulation of NCAM polysialylation is associated with morphofunctional modifications in the hypothalamo-neurohypophysial system during lactation. Eur. J. Neurosci. 9:1997;1553-1565
51. Oka Y., Satou M., Ueda K. Descending pathways to the spinal cord in the hime salmon (landlocked red salmon, Oncorhynchus nerka). J. Comp. Neurol. 254:1986;91-103
52. Pouwels E. On the development of the cerebellum of the trout, Salmo gairdneri: IV. Development of the pattern of connectivity. Anat. Embryol. (Berl.). 153:1978;55-65
53. Rao P.D., Jadhao A.G., Sharma S.C. Topographic organization of descending projection neurons to the spinal cord of the goldfish, Carassius auratus. Brain Res. 620:1993;211-220
54. Safaei R., Fischer I. Cloning of a cDNA encoding MAP1B in rat brain: regulation of mRNA levels during development. J. Neurochem. 52:1989;1871-1879
55. Saunders N.R., Balkwill P., Knott G., Habgood M.D., Mollgard K., Treherne J.M., Nicholls J.G. Growth of axons through a lesion in the intact CNS of fetal rat maintained in long-term culture. Proc. R. Soc. Lond., B Biol. Sci. 250:1992;171-180
56. Sharma S.C., Jadhao A.G., Rao P.D. Regeneration of supraspinal projection neurons in the adult goldfish. Brain Res. 620:1993;221-228
57. Soares S., Fischer I., Ravaille-Veron M., Vincent J.D., Nothias F. Induction of MAP1B phosphorylation in target-deprived afferent fibers after kainic acid lesion in the adult rat. J. Comp. Neurol. 396:1998;193-210
58. Soares S., Von Boxberg Y., Lombard M.C., Ravaille-Veron M., Fischer I., Eyer J., Nothias F. Phosphorylated MAP1B is induced in central sprouting of primary afferents in response to peripheral injury but not in response to rhizotomy. Eur. J. Neurosci. 16:2002;593-606
59. Strata P., Tempia F., Zagrebelsky M., Rossi F. Reciprocal trophic interactions between climbing fibres and Purkinje cells in the rat cerebellum. Prog. Brain Res. 114:1997;263-282
60. Sullivan S.A., Barthel L.K., Largent B.L., Raymond P.A. A goldfish Notch-3 homologue is expressed in neurogenic regions of embryonic, adult, and regenerating brain and retina. Dev. Genet. 20:1997;208-223
61. Tomasiewicz H.G., Wood J.G. Characterization of microtubule-associated proteins in teleosts. Cell Motil. Cytoskelet. 44:1999;155-167
62. Treherne J.M., Woodward S.K., Varga Z.M., Ritchie J.M., Nicholls J.G. Restoration of conduction and growth of axons through injured spinal cord of neonatal opossum in culture. Proc. Natl. Acad. Sci. U. S. A. 89:1992;431-434
63. Tucker R.P. The roles of microtubule-associated proteins in brain morphogenesis: a review. Brain Res. Rev. 15:1990;101-120
64. Ulloa L., Avila J., Diaz-Nido J. Heterogeneity in the phosphorylation of microtubule-associated protein MAP1B during rat brain development. J. Neurochem. 61:1993;961-972
65. Ulloa L., Ibarrola N., Avila J., Diez-Guerra F.J. Microtubule-associated protein 1B (MAP1B) is present in glial cells phosphorylated different than in neurones. Glia. 10:1994;266-275
66. Vecino E., Avila J. Distribution of the phosphorylated form of microtubule associated protein 1B in the fish visual system during optic nerve regeneration. Brain Res. Bull. 56:2001;131-137
67. Vecino E., Ulloa L., Avila J. The phosphorylated isoform of microtubule associated protein 1B (MAP1B) is expressed in the visual system of the tench (Tinca tinca, L) during optic nerve regeneration. Neurosci. Lett. 245:1998;93-96
68. Vouyiouklis D.A., Brophy P.J. Microtubule-associated protein MAP1B expression precedes the morphological differentiation of oligodendrocytes. J. Neurosci. Res. 35:1993;257-267
69. Wang X.M., Terman J.R., Martin G.F. Evidence for growth of supraspinal axons through the lesion after transection of the thoracic spinal cord in the developing opossum Didelphis virginiana. J. Comp. Neurol. 371:1996;104-115
70. Weatherley A.H., Gill H.S. Press A. The Biology of Fish Growth. 1987;147-173 Academic Press, London
71. Williams D.K., Cohan C.S. The role of conditioning factors in the formation of growth cones and neurites from the axon stump after axotomy. Brain Res. Dev. Brain Res. 81:1994;89-104
72. Wullimann M.F., Northcutt R.G. Connections of the corpus cerebelli in the green sunfish and the common goldfish: a comparison of perciform and cypriniform teleosts. Brain Behav. Evol. 32:1988;293-316
73. Wullimann M.F., Rupp B., Reichert H. Neuroanatomy of the Zebrafish Brain: A Topological Atlas. 1996;Birkhauser, Basel
74. Zottoli S.J., Marek L.E., Agostini M.A., Strittmatter S.L. Morphological and physiological survival of goldfish Mauthner axons isolated from their somata by spinal cord crush. J. Comp. Neurol. 255:1987;272-282
75. Zottoli S.J., Bentley A.P., Feiner D.G., Hering J.R., Prendergast B.J., Rieff H.I. Spinal cord regeneration in adult goldfish: implications for functional recovery in vertebrates. Prog. Brain Res. 103:1994;219-228
76. Zupanc G.K., Horschke I. Proliferation zones in the brain of adult gymnotiform fish: a quantitative mapping study. J. Comp. Neurol. 353:1995;213-233
77. Zupanc G.K., Zupanc M.M. Birth and migration of neurons in the central posterior/prepacemaker nucleus during adulthood in weakly electric knifefish (Eigenmannia sp.). Proc. Natl. Acad. Sci. U. S. A. 89:1992;9539-9543